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"Jerusalem's Lot" is an epistolary short story set in the fictional town of Preacher's Corners, Cumberland County, Maine, in 1850. It is told through a series of letters and diary entries, mainly those of its main character, aristocrat Charles Boone, although his manservant, Calvin McCann, also occasionally assumes the role of narrator.

Charles Boone, in letters addressed to "Bones", describes the arrival of himself and his manservant, Calvin McCann, at Chapelwaite, the neglected ancestral home of Charles's estranged dead cousin. Calvin learns that many people in the nearby Maine town of Preacher's Corners think Charles and Calvin are mad for living in the mansion. The house is said to be "a bad house", with a history of sad events, disappearances, and mysterious noises which Charles attributes to "rats in the walls". Calvin finds a hidden compartment in the library containing an old map of a deserted village called Jerusalem's Lot, a mysterious area the townsfolk avoid. Their curiosity piqued, Charles and Calvin set out to explore the village.

The two men find a decayed Puritan settlement. Nothing has set foot in the town since its abandonment, including animals. As the two men explore a nearby church, they discover an obscene parody of the Madonna and Child and an inverted cross. At the pulpit, they find a book filled with Latin and Druidicrunes entitled De Vermis Mysteriis, or "The Mysteries of the Worm". When Charles touches the book, the church shakes and the two men feel something gigantic moving in the ground beneath them. The evil of the place overcomes both men, and they quickly leave the village.

The inhabitants of Preacher's Corners begin fearing Charles. He is chased away from one house with rocks and guns. Charles asks Mrs. Cloris, Chapelwaite's former maid, for information about Jerusalem's Lot. She reveals that a rift in Charles' family was caused when his grandfather, Robert Boone, attempted to steal De Vermis Mysteriis from his brother, Philip, presumably to destroy it. Philip was a minister heavily involved in the occult who, on October 31, 1789, vanished along with the population of Jerusalem's Lot. Charles dismisses it as superstition, but cannot forget what he saw in the church.

Calvin discovers a diary in the library, encrypted with a rail fence cipher. Before he can decipher it, Charles takes him into the cellar to check for rats. Hidden behind the walls they find the ancient, undead corpses of two of his relatives, Marcella and Randolph Boone. Charles recognizes them as "nosferatu". The two men flee the cellar, and Calvin seals the trapdoor to prevent any pursuit from the creatures.

As Charles recovers from the encounter, Calvin cracks the cipher. The diary, written by Robert Boone, details the history of Jerusalem's Lot and the events leading up to the mass disappearance. The village was founded by one of Charles' distant ancestors, James Boon, who was the leader of an inbredwitchcraftcult. Philip and Robert took up residence in Chapelwaite, Philip was taken in by Boon's cult, and acquired De Vermis Mysteriis at Boon's behest. Philip and Boon used the book to call forth a supernatural entity referred to as "The Worm". In his final entry, Robert curses the whip-poor-will birds that have descended upon Chapelwaite.

Charles feels compelled to return to Jerusalem's Lot. Calvin attempts to prevent it, but eventually relents, accompanying his master. They discover a butchered lamb on the church altar, lying on top of De Vermis Mysteriis. Charles moves the lamb and takes the book, intending to destroy it, but a congregation of undead appears, including Philip and Boon. Charles becomes possessed and begins chanting, summoning forth the Worm. Calvin knocks down Charles, freeing him from possession. Charles sets fire to the book. The Worm lashes out from below, killing Calvin before disappearing. Before Charles can recover Calvin's body, Boon forces Charles to flee. In his final letter to "Bones", Charles announces his intention to commit suicide, ending the Boone family line.

An "editor's note" attributes Charles's letters and the death of Calvin to insanity rather than supernatural occurrences in Jerusalem's Lot. The editor notes that Charles was not the last of his line: a bastard relative still exists—the editor himself, James Robert Boone, who has moved to Chapelwaite to restore the family name. James notes that Charles was right about one thing: "This place badly needs the services of an exterminator. There are some huge rats in the walls, by the sound." The note is dated October 2, the same date as Charles's first letter.